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Variation in Inbreeding Depression Among Families and Populations of Clarkia Tembloriensis (Onagraceae)

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Variation in Inbreeding Depression Among Families and Populations of Clarkia Tembloriensis (Onagraceae) Heredity 76 (1996) 83—91 Received 9 June 1995 Variation in inbreeding depression among families and populations of Clarkia tembloriensis (Onagraceae) TIMOTHY P. HOLTSFORD Division of Biological Sciences, University of Missouri, Columbia, MO 65203, U.S.A. Therelationship between the self-fertilization rate of a population and the severity of inbreed- ing depression is difficult to predict because the underlying genetics may be complex. However, it is important to understand this relationship, and the degree to which inbreeding depression varies among families within populations, if we are to understand the evolution of plant mating systems. Inbreeding depression was studied in glasshouse trials using seed derived from two populations of Clarkia tembloriensis, Cantua Creek and Idria. These had very different rates of self-fertilization (s) and inbreeding coefficients (F) (s =0.74,F =0.77in the CC-i population; s =0.i6,F 0.10 in the I-i population). Outcrossing between these populations was equivalent to outcrossing within them; there was no evidence for outbreeding depression or increased heterosis from interpopulation crosses. The more self-fertilizing CC-i population had fewer recessive lethal genes than the outbreeding I-i population. However, cumulative inbreeding depression at the end of flowering was not significantly different between these populations. Inbreeding has seemingly purged the lethal genes from the CC-i population but overall mutational load, especially in characters that are manifest late in the life history, is still substantial despite a history of inbreeding. Variation in inbreeding depression among families within these two populations was surprisingly large. The range of variation among families was five to seven times larger than the difference in inbreeding depression between populations. Variation in inbreeding depression among families should make these populations more susceptible to the invasion of genes which increase the rate of self-fertilization. Keywords:Clarkia,inbreeding depression, mating system, self-fertilization. increased homozygosity can be detrimental if the Introduction alleles at individual loci affecting fitness have a Individualswhose parents are related by descent are synergistic overdominant interaction so that hetero- often less vigorous than individuals whose parents zygotes are always more fit than homozygotes. If are unrelated. The decrease in fitness of inbred inbreeding depression is caused by the expression of progeny relative to outbred progeny is termed deleterious recessive alleles then natural selection inbreeding depression. Inbreeding depression is an can decrease the severity of inbreeding depression important phenomenon because it can affect the over successive generations of inbreeding. However, evolution of plant mating systems, the speed and the rate at which deleterious recessives are elimi- efficacy of plant breeding programmes and the nated from populations and the equilibrium fre- choice of strategy employed to sample or preserve quencies of these alleles depend on several genetic diversity of rare or endangered populations. parameters. The number of gene loci, the degree The genetic basis of inbreeding depression will and kinds of interactions between loci, the rate of determine how inbreeding depression can coevolve mutation, the strength of selection, and the domi- with the mating system. Increased homozygosity can nance coefficients of genes affecting fitness may all lead to inbreeding depression by two different be important in determining the severity of inbreed- genetic mechanisms. Homozygosity can cause dele- ing depression (Charlesworth & Charlesworth, 1990; terious recessive or partially recessive alleles to show Charlesworth et al., i990, 199i). If inbreeding their effects on the phenotype. Alternatively, depression results from the loss of overdominant 1996 The Genetical Society of Great Britain. 83 84 T. P. HOLTSFORD allelic interactions as homozygosity increases then families for fitness-determining genes may allow the evolution of inbreeding depression will follow a genes for self-fertilization to invade an outbreeding different course (Charlesworth & Charlesworth, population despite high average population inbreed- 1990). If the overdominance is asymmetrical (i.e. ing depression, because selfing genes will become one allele confers a higher average fitness than its associated with high viability genes (Uyenoyama & alternative) then inbreeding depression should Wailer, 1991a). If there is overdominance for fitness decline to zero as the mating system approaches then variation in inbreeding depression among complete self-fertilization because if homozygosity is families will allow outcrossing genes to become inescapable then the allele that performs better associated with high viability genes (Uyenoyama & when homozygous will become fixed. Symmetrical WaIler, 1991b). The associations between genes overdominance, though unlikely, would lead to an influencing the mating system and genes influencing increase in inbreeding depression as self-fertilization fitness may have as much or more effect on the increases, heterozygotes become rare and both course of mating system evolution as the magnitude homozygotes are equally unfit (Charlesworth & of inbreeding depression (Holsinger, 1988; Ueyno- Charlesworth, 1990). yama & Wailer, 1991a,b,c). The degree to which a history of inbreeding modi- This paper was motivated by these shortcomings fies the severity of inbreeding depression is an issue in our empirical knowledge: does a history of on which empirical data are few and confusing inbreeding result in the purging of mutational load, (Toppings, 1989; Holtsford & Ellstrand, 1990; and is there significant variation among families in Rathcke & Real, 1993; Eckert & Barrett, 1994; the severity of inbreeding depression? I also ask Latta & Ritland, 1994; McCall et at., 1994). No clear whether outcrossing between populations results in picture has emerged on the degree to which muta- more heterosis (the complement of inbreeding tional load may be purged by the increased effi- depression), than outcrossing within populations, or ciency of selection acting on more homozygous whether crossing between populations results in inbred populations. Although selection should be outbreeding depression (Price & Waser, 1979; more efficient at decreasing the frequency of delete- Waser & Price, 1991; Waser, 1992). The Cantua rious recessives when those genes are homozygous, Creek-i (CC-i) and Idria-i (I-i) populations of highly inbred populations may still show substantial Clarkia tembloriensis were chosen for this study inbreeding depression (Karron, 1989; Holtsford & because their mating systems and inbreeding coeffi- Ellstrand, 1990; Johnston, 1992). Purging of delete- cients are quite different (selfing rates, s =0.74and rious recessive genes should be more difficult when 0.16; inbreeding coefficients, F =0.77and 0.10, population sizes are small enough so that drift may respectively; Holtsford & Elistrand, 1989), and increase the frequency of these genes, when the because the genetic basis of the floral traits under- deleterious alleles are more recessive, and have lying the mating system differences in these popula- smaller individual effects on fitness (Charlesworth & tions have been studied (Holtsford & Ellstrand, Charlesworth, 1987; Charlesworth et at., 1990). 1992). Furthermore, even recessive lethals may not be purged unless inbreeding exceeds a threshold value, which may be surprisingly high, even for moderate Materialsand methods mutation rates (Lande et a!., 1994). High mutation Thestudy populations occur 36 km apart in the rates to deleterious recessive alleles would also inner coast ranges of central California, U.S.A. impede the purging of mutational load (Johnston & (Idria-1: 36°33'OO"N, 120°50'OO"W, 457 m altitude, Schoen, 1995 and references therein). Cantua Cr-i: 36°24'30"N, i20°28'30"W, 366 m). Another unresolved issue is how much inbreeding Voucher specimens are deposited at the herbaria of depression varies among families within populations. the Universities of California, Riverside and Inter-family variation in mutational load should be Missouri. The mating system and structure of these critically important to mating system evolution populations is described elsewhere (Holtsford & (Uyenoyama & Wailer, 1991a,b,c). In partially Elistrand, 1989). Ten seeds from each of iS mater- inbreeding populations identity disequilibria will nal parents from the CC-i and I-i populations were develop among loci influencing the mating system sown on vermiculite and placed in a growth chamber and loci influencing fitness (Weir & Cockerham, (12 h light: 12 h dark, 24°C day, 7°C night). When 1973; Holsinger, 1988; Uyenoyama & Wailer, the first set of true leaves appeared, one seedling 1991a,b,c). If inbreeding depression is caused by from each field-collected maternal plant was trans- deleterious recessive genes then variation among planted into a 5 cm square pot and the seedlings The Genetical Society of Great Britain, Heredity, 76, 83—91. VARIATION IN INBREEDING DEPRESSION IN CLARK/A 85 were moved to a glasshouse. The seedlings were root axis. The number of flowers, rather than the transplanted to 10 cm diameter pots when they were number of fruits or seeds, was used as an estimate of 15 cm tall and into 4 L pots when they were reproductive effort because the CC-i population is 30—40 cm tall. highly autogamous whereas I-i sets very few seeds in All plants received
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